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<select id="email-citation-format" name="citation-format" class="action-panel-selector email-citation-format">
<option selected="selected" value="summary">Summary</option>
<option value="summary-text">Summary (text)</option>
<option value="abstract">Abstract</option>
<option value="abstract-text">Abstract (text)</option>
</select>
</div>
<div class="include-supplemental-container">
<input type="checkbox" aria-label="Include MeSH and other data" name="include-supplemental" id="email-include-supplemental" class="email-include-supplemental">
<label for="email-include-supplemental" class="email-include-supplemental-label">MeSH and other data</label>
</div>
<div class="form-field recaptcha ">
<div class="g-recaptcha" id="id-recaptcha" data-sitekey="6LfsWHMdAAAAAClKbtOpjQ2pMjgsGxvv7NdZW9uI"></div>
</div>
<div id="captcha-error-message" class="usa-input-error-message captcha-validation-message" role="alert"></div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Sending..."
data-ga-category="save_share"
data-ga-action="email"
data-ga-label="send">
Send email
</button>
<button class="action-panel-cancel"
aria-label="Close 'Email citations' panel"
ref="linksrc=close_email_panel"
aria-controls="email-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="email"
data-ga-label="cancel">
Cancel
</button>
</div>
<input type="hidden" name="email-search-details" value="" />
<input type="hidden" name="email-search-details-hash" value="0e42663a6c3bd85498fcb88798998fed7bfdc45d457db35281e41afe13cc0524" />
</form>
</div>
</div>
<div id="collections-action-panel"
class="collections-action-panel action-panel in-progress-dots-panel"
aria-hidden="true"
data-collections-open-panel-enabled="false"
data-collections-open-panel-url-hash="#open-collections-panel">
<div class="inner-wrap">
<h3 class="action-panel-heading">
Add to Collections
</h3>
<form id="collections-action-panel-form"
class="collections-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
data-existing-collections-url="/list-existing-collections/"
data-add-to-existing-collection-url="/add-to-existing-collection/"
data-create-and-add-to-new-collection-url="/create-and-add-to-new-collection/"
data-get-article-ids-by-search-url="/get-article-ids-by-search/"
data-myncbi-max-collection-name-length="100"
data-add-to-collection-max-amount="1000"
data-collections-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/">
<input type="hidden" name="csrfmiddlewaretoken" value="B1bYHp3IYeGk0tOryUa61GK7YlMqYnKdSOV3kfw4yPtOUUUhbdN8vOgLwpuCRYix">
<div class="choice-group" role="radiogroup">
<ul class="radio-group-items">
<li>
<input type="radio"
id="collections-action-panel-new"
class="collections-new"
name="collections"
value="new"
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="collections_radio_new">
<label for="collections-action-panel-new">Create a new collection</label>
</li>
<li>
<input type="radio"
id="collections-action-panel-existing"
class="collections-existing"
name="collections"
value="existing"
checked="true"
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="collections_radio_existing">
<label for="collections-action-panel-existing">Add to an existing collection</label>
</li>
</ul>
</div>
<div class="controls-wrapper">
<div class="action-panel-control-wrap new-collections-controls">
<label for="collections-action-panel-add-to-new" class="action-panel-label required-field-asterisk">
Name your collection:
</label>
<input
type="text"
name="add-to-new-collection"
id="collections-action-panel-add-to-new"
class="collections-action-add-to-new"
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/"
maxlength="100"
data-ga-category="save_share"
data-ga-action="create_collection"
data-ga-label="non_favorties_collection">
<div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
Name must be less than 100 characters
</div>
</div>
<div class="action-panel-control-wrap existing-collections-controls">
<label for="collections-action-panel-add-to-existing" class="action-panel-label">
Choose a collection:
</label>
<select id="collections-action-panel-add-to-existing"
class="action-panel-selector collections-action-add-to-existing"
data-ga-category="save_share"
data-ga-action="select_collection"
data-ga-label="($('#collections-action-add-to-existing').val() === 'Favorites') ? 'Favorites' : 'non_favorites_collection'">
</select>
<div class="collections-retry-load-on-error usa-input-error-message selection-validation-message">
Unable to load your collection due to an error<br>
<a href="#">Please try again</a>
</div>
</div>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Adding..."
data-pinger-ignore
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="add">
Add
</button>
<button class="action-panel-cancel"
aria-label="Close 'Add to Collections' panel"
ref="linksrc=close_collections_panel"
aria-controls="collections-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="collections"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="bibliography-action-panel"
class="bibliography-action-panel action-panel in-progress-dots-panel"
aria-hidden="true"
data-bibliography-open-panel-enabled="false"
data-bibliography-open-panel-url-hash="#open-bibliography-panel">
<div class="inner-wrap">
<h3 class="action-panel-heading">
Add to My Bibliography
</h3>
<form id="bibliography-action-panel-form"
class="bibliography-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
data-add-to-bibliography-max-amount="100"
data-add-to-bibliography-batch-size="10"
data-bibliography-delegates-url="/list-bibliography-delegates/"
data-add-to-bibliography-url="/add-to-bibliography/"
data-get-article-ids-by-search-url="/get-article-ids-by-search/"
data-mybib-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/mybibliography/">
<input type="hidden" name="csrfmiddlewaretoken" value="B1bYHp3IYeGk0tOryUa61GK7YlMqYnKdSOV3kfw4yPtOUUUhbdN8vOgLwpuCRYix">
<div class="action-panel-control-wrap bibliographies-controls">
<div class="choice-group">
<ul class="bibliographies-action-add radio-group-items">
<li>
<input name="bibliography" id="my-bibliography" class="my-bibliography" type="radio" checked/>
<label for="my-bibliography">My Bibliography</label>
</li>
</ul>
</div>
</div>
<div class="bibliographies-retry-load-on-error usa-input-error-message selection-validation-message">
Unable to load your delegates due to an error<br>
<a href="#">Please try again</a>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Adding..."
data-pinger-ignore>
Add
</button>
<button class="action-panel-cancel"
aria-label="Close 'Add to bibliography' panel"
ref="linksrc=close_bibliography_panel"
aria-controls="bibliography-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="mybib"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="saved-search-action-panel" class="saved-search-action-panel action-panel " aria-hidden="true"
data-saved-search-open-panel-enabled="false"
data-saved-search-open-panel-url-hash="#open-saved-search-panel">
<div class="inner-wrap">
<h2 class="action-panel-heading">
Your saved search
</h2>
<form id="saved-search-action-panel-form"
class="saved-search-action-panel-form action-panel-content action-form"
data-create-saved-search-url="/create-saved-search/"
data-try-search-terms-url="/try-search-term/"
data-saved-search-root-url="https://www.ncbi.nlm.nih.gov/myncbi/searches/">
<input type="hidden" name="csrfmiddlewaretoken" value="B1bYHp3IYeGk0tOryUa61GK7YlMqYnKdSOV3kfw4yPtOUUUhbdN8vOgLwpuCRYix">
<div class="action-panel-control-wrap">
<label for="saved-search-name" class="action-panel-label saved-search-name-label required-field-asterisk">
Name of saved search:
</label>
<input maxlength="200"
type="text"
name="saved-search-name"
id="saved-search-name"
class="saved-search-name"
value=""
required
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/">
</div>
<div class="action-panel-control-wrap">
<label for="saved-search-term" class="action-panel-label required-field-asterisk">
Search terms:
</label>
<textarea name="saved-search-term" id="saved-search-term" class="saved-search-term" required></textarea>
</div>
<div class="test-search-term-wrap">
<a href="#" class="try-search-term">Test search terms</a>
</div>
<div class="choice-group action-panel-extra-margin-top">
<span class="action-panel-label" id="fieldset-label">
Would you like email updates of new search results?
</span>
<fieldset id="saved-search-alert" aria-describedby="fieldset-label">
<legend class="usa-sr-only">Saved Search Alert Radio Buttons</legend>
<ul class="radio-group-items">
<li>
<input type="radio" id="saved-search-alert-yes" class="saved-search-alert-yes" name="saved-search-alert" value="yes" checked>
<label for="saved-search-alert-yes" class="action-panel-label">Yes</label>
</li>
<li>
<input aria-label="No radio input" type="radio" id="saved-search-alert-no" class="saved-search-alert-no" name="saved-search-alert" value="no">
<label for="saved-search-alert-no" class="action-panel-label">No</label>
</li>
</ul>
</fieldset>
</div>
<div class="alert-schedule-wrap">
<div class="action-panel-control-wrap">
<label class="action-panel-label">
Email:
</label>
<span aria-label="Email address" id="saved-search-email" class="action-panel-label"><span class="action-panel-label-bold"></span> (<a class="myncbi-account-settings" href="https://www.ncbi.nlm.nih.gov/account/settings/">change</a>)</span>
</div>
<div class="action-panel-control-wrap action-panel-extra-margin-top">
<label for="saved-search-frequency" class="action-panel-label">
Frequency:
</label>
<select id="saved-search-frequency" class="no-border-panel-selector saved-search-frequency">
<option value="monthly">Monthly</option>
<option value="weekly">Weekly</option>
<option value="daily">Daily</option>
</select>
</div>
<div class="action-panel-control-wrap saved-search-monthly-additional">
<label for="saved-search-monthly-on-day" class="action-panel-label">
Which day?
</label>
<select id="saved-search-monthly-on-day" class="no-border-panel-selector">
<option value="Sunday">The first Sunday</option>
<option value="Monday">The first Monday</option>
<option value="Tuesday">The first Tuesday</option>
<option value="Wednesday">The first Wednesday</option>
<option value="Thursday">The first Thursday</option>
<option value="Friday">The first Friday</option>
<option value="Saturday">The first Saturday</option>
<option value="day">The first day</option>
<option value="weekday">The first weekday</option>
</select>
</div>
<div class="action-panel-control-wrap saved-search-weekly-additional">
<label for="saved-search-weekly-on-day" class="action-panel-label">
Which day?
</label>
<select id="saved-search-weekly-on-day" class="no-border-panel-selector saved-search-weekly-on-day">
<option value="Sunday">Sunday</option>
<option value="Monday">Monday</option>
<option value="Tuesday">Tuesday</option>
<option value="Wednesday">Wednesday</option>
<option value="Thursday">Thursday</option>
<option value="Friday">Friday</option>
<option value="Saturday">Saturday</option>
</select>
</div>
<div class="action-panel-control-wrap">
<label for="saved-search-report" class="action-panel-label">
Report format:
</label>
<select id="saved-search-report" class="no-border-panel-selector saved-search-report">
<option value="DocSum">Summary</option>
<option value="DocSumText">Summary (text)</option>
<option value="Abstract">Abstract</option>
<option value="AbstractText">Abstract (text)</option>
<option value="MEDLINE">PubMed</option>
</select>
</div>
<div class="action-panel-control-wrap">
<label for="saved-search-amount" class="action-panel-label">
Send at most:
</label>
<select id="saved-search-amount" class="no-border-panel-selector saved-search-amount">
<option value="1">1 item</option>
<option value="5" selected>5 items</option>
<option value="10">10 items</option>
<option value="20">20 items</option>
<option value="50">50 items</option>
<option value="100">100 items</option>
<option value="200">200 items</option>
</select>
</div>
<div>
<input type="checkbox" id="saved-search-send-if-no-result" class="saved-search-send-if-no-result" name="saved-search-send-if-no-result">
<label for="saved-search-send-if-no-result" class="action-panel-label smaller-checkbox">
Send even when there aren't any new results
</label>
</div>
<div class="action-panel-control-wrap option-text-in-email-wrap">
<label for="saved-search-email-text" class="action-panel-label">
Optional text in email:
</label>
<textarea name="saved-search-email-text"
id="saved-search-email-text"
class="saved-search-email-text"></textarea>
</div>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Saving..."
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="save">
Save
</button>
<button class="action-panel-cancel"
aria-label="Close 'Your saved search' panel"
ref="linksrc=close_saved_search_panel"
aria-controls="saved-search-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="citation-manager-action-panel" class="citation-manager-action-panel action-panel" aria-hidden="true">
<div class="inner-wrap">
<h2 class="action-panel-heading">
Create a file for external citation management software
</h2>
<form id="citation-manager-action-panel-form"
class="action-panel-content action-form"
action="/results-export-ids/"
data-by-search-action="/results-export-search-data/"
data-by-ids-action="/results-export-ids/"
method="post"
data-by-search-method="post"
data-by-ids-method="post">
<input type="hidden" name="csrfmiddlewaretoken" value="B1bYHp3IYeGk0tOryUa61GK7YlMqYnKdSOV3kfw4yPtOUUUhbdN8vOgLwpuCRYix">
<input name="results-format" type="hidden" value="pubmed"/>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Sending..."
data-ga-category="save_share"
data-ga-action="citation_manager"
data-ga-label="save">
Create file
</button>
<button class="action-panel-cancel"
aria-label="Close 'Send citations to citation manager' panel"
ref="linksrc=close_citation_manager_panel"
aria-controls="citation-manager-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="citation_manager"
data-ga-label="cancel">
Cancel
</button>
</div>
</form>
</div>
</div>
<div id="rss-action-panel" class="rss-action-panel action-panel " aria-hidden="true">
<div class="inner-wrap">
<h2 class="action-panel-heading">
Your RSS Feed
</h2>
<form id="rss-action-panel-form"
class="rss-action-panel-form action-panel-content action-form"
data-create-rss-feed-url="/create-rss-feed-url/"
data-search-form-term-value="">
<input type="hidden" name="csrfmiddlewaretoken" value="B1bYHp3IYeGk0tOryUa61GK7YlMqYnKdSOV3kfw4yPtOUUUhbdN8vOgLwpuCRYix">
<div class="action-panel-control-wrap">
<label for="rss-name" class="action-panel-label required-field-asterisk">
Name of RSS Feed:
</label>
<input maxlength="200"
placeholder="Name"
type="text"
name="rss-name"
id="rss-name"
class="rss-name"
value=''
required
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/">
</div>
<div class="rss-limit-wrap">
<div class="action-panel-control-wrap action-panel-extra-margin-top">
<label for="rss-limit" class="action-panel-label">
Number of items displayed:
</label>
<select id="rss-limit" class="no-border-panel-selector rss-limit">
<option value="5">5</option>
<option value="10">10</option>
<option value="15" selected="selected">15</option>
<option value="20">20</option>
<option value="50">50</option>
<option value="100">100</option>
</select>
</div>
</div>
<div class="action-panel-actions">
<button class="action-panel-submit"
type="submit"
data-loading-label="Creating..."
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="save">
Create RSS
</button>
<button class="action-panel-cancel"
aria-label="Close 'Your RSS' panel"
ref="linksrc=close_rss_panel"
aria-controls="rss-action-panel"
aria-expanded="false"
data-ga-category="save_share"
data-ga-action="alert"
data-ga-label="cancel">
Cancel
</button>
</div>
<div class="action-panel-control-wrap rss-link-copy-wrap">
<label for="rss-link" class="usa-sr-only">RSS Link</label>
<input placeholder="Your RSS Feed Link" type="text" name="rss-link" id="rss-link" class="rss-link" title="RSS Link">
<button
type="button"
disabled
class="rss-link-copy-button disabled"
data-ga-category="save_share"
data-ga-action="rss"
data-ga-label="copy">
Copy
</button>
</div>
</form>
</div>
</div>
</div>
</div>
<div class="article-page" id="article-page" data-article-pmid="37055935">
<aside class="page-sidebar">
<div class="inner-wrap">
<div class="full-text-links">
<div class="full-view">
<h3 class="title">
Full text links
</h3>
<div class="full-text-links-list">
<a class="link-item
dialog-focus"
href="https://www.tandfonline.com/doi/abs/10.1080/15548627.2023.2200554?url_ver=Z39.88-2003&amp;rfr_id=ori:rid:crossref.org&amp;rfr_dat=cr_pub 0pubmed"
target="_blank"
rel="noopener"
ref="linksrc=fulltextorjournal_fulltext&amp;is_pmc=False&amp;PrId=4487&amp;itool=Abstract-def&amp;log$=linkouticon&amp;uid=37055935&amp;db=pubmed&amp;nlmid=101265188"
title="See full text options at Atypon"
data-ga-category="full_text"
data-ga-action="Atypon"
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Atypon
</span></a><a class="link-item
pmc
"
href="https://pmc.ncbi.nlm.nih.gov/articles/pmid/37055935/"
target="_blank"
rel="noopener"
ref="linksrc=fulltextorjournal_fulltext&amp;is_pmc=True&amp;PrId=3494&amp;itool=Abstract-def&amp;log$=linkouticon&amp;uid=37055935&amp;db=pubmed&amp;nlmid=101265188"
title="Free full text at PubMed Central"
data-ga-category="full_text"
data-ga-action="PMC"
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><span class="text">
Free PMC article
</span></a>
</div>
</div>
<div class="short-view">
<a href="#" class="full-text-links-button full-text-links-dialog-trigger">
Full text links
</a>
</div>
</div>
<div class="actions-buttons sidebar"><h3 class="title">Actions</h3><div class="inner-wrap"><button class="citation-button citation-dialog-trigger"
aria-label="Open dialog with citation text in different styles"
data-ga-category="save_share"
data-ga-action="cite"
data-ga-label="open"
data-all-citations-url="/37055935/citations/"
data-citation-style="nlm"
data-pubmed-format-link="/37055935/export/"><span class="button-label">Cite</span></button><link type="text/css" href="ncbi-overlay-block/src/overlay-block.css"><div class="collections-button-container" data-article-id="37055935" data-article-db="pubmed"><button class="collections-button collections-dialog-trigger"
aria-label="Save article in MyNCBI collections."
data-ga-category="collections_button"
data-ga-action="click"
data-ga-label="collections_button"
data-collections-open-dialog-enabled="false"
data-collections-open-dialog-url="https://account.ncbi.nlm.nih.gov/?back_url=https%3A%2F%2Fpubmed.ncbi.nlm.nih.gov%2F37055935%2F%23open-collections-dialog"
data-in-collections="false"><span class="button-label">Collections</span></button><div class="overlay" role="dialog"><div id="collections-action-dialog"
class="dialog collections-dialog"
aria-hidden="true"><div class="title">Add to Collections</div><div class="collections-action-panel action-panel"><form id="collections-action-dialog-form"
class="collections-action-panel-form action-panel-content action-form action-panel-smaller-selectors"
data-existing-collections-url="/list-existing-collections/"
data-add-to-existing-collection-url="/add-to-existing-collection/"
data-create-and-add-to-new-collection-url="/create-and-add-to-new-collection/"
data-myncbi-max-collection-name-length="100"
data-collections-root-url="https://www.ncbi.nlm.nih.gov/myncbi/collections/"><input type="hidden" name="csrfmiddlewaretoken" value="B1bYHp3IYeGk0tOryUa61GK7YlMqYnKdSOV3kfw4yPtOUUUhbdN8vOgLwpuCRYix"><div class="choice-group" role="radiogroup"><ul class="radio-group-items"><li><input type="radio"
id="collections-action-dialog-new"
class="collections-new"
name="collections"
value="new"
data-ga-category="collections_button"
data-ga-action="click"
data-ga-label="collections_radio_new"><label for="collections-action-dialog-new">Create a new collection</label></li><li><input type="radio"
id="collections-action-dialog-existing"
class="collections-existing"
name="collections"
value="existing"
checked="true"
data-ga-category="collections_button"
data-ga-action="click"
data-ga-label="collections_radio_existing"><label for="collections-action-dialog-existing">Add to an existing collection</label></li></ul></div><div class="controls-wrapper"><div class="action-panel-control-wrap new-collections-controls"><label for="collections-action-dialog-add-to-new" class="action-panel-label required-field-asterisk">
Name your collection:
</label><input
type="text"
name="add-to-new-collection"
id="collections-action-dialog-add-to-new"
class="collections-action-add-to-new"
pattern="[^&quot;&amp;=&lt;&gt;\/]*" title="The following characters are not allowed in the Name field: &quot;&amp;=&lt;&gt;/"
maxlength="100"
data-ga-category="collections_button"
data-ga-action="create_collection"
data-ga-label="non_favorties_collection"><div class="collections-new-name-too-long usa-input-error-message selection-validation-message">
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><sup class="key">1</sup> Guangzhou Municipal and Guangdong Provincial Key Laboratory of Protein Modification and Degradation, State Key Laboratory of Respiratory Disease, School of Basic Medical Sciences, Affliated Cancer Hospital &amp; Institute of Guangzhou Medical University, Guangzhou, China.</li>
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><sup class="key">2</sup> Department of Surgery, UT Southwestern Medical Center, Dallas, TX, USA.</li>
<li data-affiliation-id="short-view-affiliation-3"
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><sup class="key">3</sup> Life Sciences Institute and Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI, USA.</li>
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Copper is an essential trace element in biological systems, maintaining the activity of enzymes and the function of transcription factors. However, at high concentrations, copper ions show increased toxicity by inducing regulated cell death, such as apoptosis, paraptosis, pyroptosis, ferroptosis, and cuproptosis. Furthermore, copper ions can trigger macroautophagy/autophagy, a lysosome-dependent degradation pathway that plays a dual role in regulating the survival or death fate of cells under various stress conditions. Pathologically, impaired copper metabolism due to environmental or genetic causes is implicated in a variety of human diseases, such as rare Wilson disease and common cancers. Therapeutically, copper-based compounds are potential chemotherapeutic agents that can be used alone or in combination with other drugs or approaches to treat cancer. Here, we review the progress made in understanding copper metabolic processes and their impact on the regulation of cell death and autophagy. This knowledge may help in the design of future clinical tools to improve cancer diagnosis and treatment.<b>Abbreviations:</b> ACSL4, acyl-CoA synthetase long chain family member 4; AIFM1/AIF, apoptosis inducing factor mitochondria associated 1; AIFM2, apoptosis inducing factor mitochondria associated 2; ALDH, aldehyde dehydrogenase; ALOX, arachidonate lipoxygenase; AMPK, AMP-activated protein kinase; APAF1, apoptotic peptidase activating factor 1; ATF4, activating transcription factor 4; ATG, autophagy related; ATG13, autophagy related 13; ATG5, autophagy related 5; ATOX1, antioxidant 1 copper chaperone; ATP, adenosine triphosphate; ATP7A, ATPase copper transporting alpha; ATP7B, ATPase copper transporting beta; BAK1, BCL2 antagonist/killer 1; BAX, BCL2 associated X apoptosis regulator; BBC3/PUMA, BCL2 binding component 3; BCS, bathocuproinedisulfonic acid; BECN1, beclin 1; BID, BH3 interacting domain death agonist; BRCA1, BRCA1 DNA repair associated; BSO, buthionine sulphoximine; CASP1, caspase 1; CASP3, caspase 3; CASP4/CASP11, caspase 4; CASP5, caspase 5; CASP8, caspase 8; CASP9, caspase 9; CCS, copper chaperone for superoxide dismutase; CD274/PD-L1, CD274 molecule; CDH2, cadherin 2; CDKN1A/p21, cyclin dependent kinase inhibitor 1A; CDKN1B/p27, cyclin-dependent kinase inhibitor 1B; COMMD10, COMM domain containing 10; CoQ10, coenzyme Q 10; CoQ10H2, reduced coenzyme Q 10; COX11, cytochrome c oxidase copper chaperone COX11; COX17, cytochrome c oxidase copper chaperone COX17; CP, ceruloplasmin; CYCS, cytochrome c, somatic; DBH, dopamine beta-hydroxylase; DDIT3/CHOP, DNA damage inducible transcript 3; DLAT, dihydrolipoamide S-acetyltransferase; DTC, diethyldithiocarbamate; EIF2A, eukaryotic translation initiation factor 2A; EIF2AK3/PERK, eukaryotic translation initiation factor 2 alpha kinase 3; ER, endoplasmic reticulum; ESCRT-III, endosomal sorting complex required for transport-III; ETC, electron transport chain; FABP3, fatty acid binding protein 3; FABP7, fatty acid binding protein 7; FADD, Fas associated via death domain; FAS, Fas cell surface death receptor; FASL, Fas ligand; FDX1, ferredoxin 1; GNAQ/11, G protein subunit alpha q/11; GPX4, glutathione peroxidase 4; GSDMD, gasdermin D; GSH, glutathione; HDAC, histone deacetylase; HIF1, hypoxia inducible factor 1; HIF1A, hypoxia inducible factor 1 subunit alpha; HMGB1, high mobility group box 1; IL1B, interleukin 1 beta; IL17, interleukin 17; KRAS, KRAS proto-oncogene, GTPase; LOX, lysyl oxidase; LPCAT3, lysophosphatidylcholine acyltransferase 3; MAP1LC3, microtubule associated protein 1 light chain 3; MAP2K1, mitogen-activated protein kinase kinase 1; MAP2K2, mitogen-activated protein kinase kinase 2; MAPK, mitogen-activated protein kinases; MAPK14/p38, mitogen-activated protein kinase 14; MEMO1, mediator of cell motility 1; MT-CO1/COX1, mitochondrially encoded cytochrome c oxidase I; MT-CO2/COX2, mitochondrially encoded cytochrome c oxidase II; MTOR, mechanistic target of rapamycin kinase; MTs, metallothioneins; NAC, N-acetylcysteine; NFKB/NF-Κb, nuclear factor kappa B; NLRP3, NLR family pyrin domain containing 3; NPLOC4/NPL4, NPL4 homolog ubiquitin recognition factor; PDE3B, phosphodiesterase 3B; PDK1, phosphoinositide dependent protein kinase 1; PHD, prolyl-4-hydroxylase domain; PIK3C3/VPS34, phosphatidylinositol 3-kinase catalytic subunit type 3; PMAIP1/NOXA, phorbol-12-myristate-13-acetate-induced protein 1; POR, cytochrome P450 oxidoreductase; PUFA-PL, PUFA of phospholipids; PUFAs, polyunsaturated fatty acids; ROS, reactive oxygen species; SCO1, synthesis of cytochrome C oxidase 1; SCO2, synthesis of cytochrome C oxidase 2; SLC7A11, solute carrier family 7 member 11; SLC11A2/DMT1, solute carrier family 11 member 2; SLC31A1/CTR1, solute carrier family 31 member 1; SLC47A1, solute carrier family 47 member 1; SOD1, superoxide dismutase; SP1, Sp1 transcription factor; SQSTM1/p62, sequestosome 1; STEAP4, STEAP4 metalloreductase; TAX1BP1, Tax1 binding protein 1; TEPA, tetraethylenepentamine; TFEB, transcription factor EB; TM, tetrathiomolybdate; TP53/p53, tumor protein p53; TXNRD1, thioredoxin reductase 1; UCHL5, ubiquitin C-terminal hydrolase L5; ULK1, Unc-51 like autophagy activating kinase 1; ULK1, unc-51 like autophagy activating kinase 1; ULK2, unc-51 like autophagy activating kinase 2; USP14, ubiquitin specific peptidase 14; VEGF, vascular endothelial gro wth factor; XIAP, X-linked inhibitor of apoptosis.
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Keywords:
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autophagy; cancer; cell death; copper; cuproptosis; ferroptosis.
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<p xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:p1="http://pubmed.gov/pub-one">No potential conflict of interest was reported by the authors.</p>
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<div class="figures" id="figures">
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Figures
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<p> Figure 1. </p>
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<div class="figure-caption-contents"><p> Dual role of copper in… </p></div>
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<p> Figure 1. </p>
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<div class="figure-caption-contents"><p> Dual role of copper in cancer development. On the one hand, elevated copper… </p></div>
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Figure 1.
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<div class="figure-caption-contents">Dual role of copper in cancer development. On the one hand, elevated copper levels can promote tumor growth by inducing ROS production, exacerbating genomic instability, and affecting various tumor-associated signal transduction events. On the other hand, excessive copper concentrations can induce tumor cell death when they exceed a certain threshold limit.</div>
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<img class="figure-thumb" itemprop="thumbnail"
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/d5293fd710f4/KAUP_A_2200554_F0002_OC.gif"
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<p> Figure 2. </p>
</strong>
<div class="figure-caption-contents"><p> Molecular mechanisms of copper metabolism.… </p></div>
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<strong class="figure-label">
<p> Figure 2. </p>
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<div class="figure-caption-contents"><p> Molecular mechanisms of copper metabolism. Copper metabolism is a complex dynamic process regulated… </p></div>
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Figure 2.
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<div class="figure-caption-contents">Molecular mechanisms of copper metabolism. Copper metabolism is a complex dynamic process regulated at the cellular and organ level by multiple molecules. The uptake of copper ions is mediated by SLC31A1 and SLC31A2, while the export of copper is driven by ATP7A and ATP7B. In cells, copper is transported to different subcellular organelles for bioavailability by several copper-binding proteins, including COX17, CCS, and ATOX1. Furthermore, the binding of MT1, MT2 and GSH to copper can limit the cytotoxicity of copper excess.</div>
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/10255ccd8828/KAUP_A_2200554_F0003_OC.gif"
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<strong class="figure-label">
<p> Figure 3. </p>
</strong>
<div class="figure-caption-contents"><p> Types of regulated cell death.… </p></div>
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 3. </p>
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<div class="figure-caption-contents"><p> Types of regulated cell death. Regulated cell death is a biologically controlled process… </p></div>
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Figure 3.
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<div class="figure-caption-contents">Types of regulated cell death. Regulated cell death is a biologically controlled process involved in various physiological or pathological events. It can be divided into apoptotic and non-apoptotic cell death. Compared with apoptosis, which generally requires the activation of caspase proteases, non-apoptotic cells are mostly caspase-independent and have the morphological characteristics of necrosis.</div>
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/9da52b97a8ba/KAUP_A_2200554_F0004_OC.gif"
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<strong class="figure-label">
<p> Figure 4. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in apoptosis.… </p></div>
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 4. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in apoptosis. (A) Mechanism of copper-induced apoptosis. Copper induces apoptosis… </p></div>
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<figcaption id="figure-caption-3" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
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Figure 4.
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<div class="figure-caption-contents">Role of copper in apoptosis. (A) Mechanism of copper-induced apoptosis. Copper induces apoptosis primarily through the induction of ROS, DNA damage, and proteasome inhibition. The apoptotic process is initiated by mitochondria-intrinsic apoptotic signals. CYCS-activated CASP9 propagates the apoptotic cascade by activating downstream CASP3, a key apoptosis execution protein that participates in the cleavage of multiple substrates. Furthermore, AIFM1 is released from mitochondria and induces caspase-independent apoptosis by attacking DNA. (B) the role of TP53 in copper-induced apoptosis. Copper induces TP53-dependent apoptosis by activating transcription of TP53 target genes, including BAX, CDKN1A/p21, PMAIP1/NOXA, and BBC3/PUMA. Copper also induces TP53-independent apoptosis by inhibiting ribosome synthesis and inducing nucleolar stress. (C, D) the anti-apoptosis role of copper. IL17 released by immune cells can increase STEAP4-mediated intracellular copper levels, leading to 5-fluorouracil (5-FU) resistance by activating the anti-apoptotic XIAP protein. Copper triggers the upregulation of CD274/PD-L1, which induces tumor immune escape by binding with PDCD1/PD-1 on activated T cells.</div>
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<p> Figure 5. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in paraptosis.… </p></div>
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<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 5. </p>
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<div class="figure-caption-contents"><p> Role of copper in paraptosis. Paraptosis is a form of regulated necrosis characterized… </p></div>
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Figure 5.
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<div class="figure-caption-contents">Role of copper in paraptosis. Paraptosis is a form of regulated necrosis characterized by vacuolation of mitochondria or ER. Copper promotes paraptosis by inducing proteasome inhibition, ER stress, Ca<sup>2+</sup> imblance, and ROS production.</div>
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src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/4db8a65af13e/KAUP_A_2200554_F0006_OC.gif"
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<p> Figure 6. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in pyroptosis.… </p></div>
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<strong class="figure-label">
<p> Figure 6. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in pyroptosis. Copper promotes pyroptosis by inducing ROS production and… </p></div>
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Figure 6.
</strong>
<div class="figure-caption-contents">Role of copper in pyroptosis. Copper promotes pyroptosis by inducing ROS production and ER stress, which leads to the formation of the NLRP3 inflammasome and the creation of membrane pores through the action of GSDMD.</div>
</figcaption>
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<p> Figure 7. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in ferroptosis.… </p></div>
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<strong class="figure-label">
<p> Figure 7. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in ferroptosis. (A) Pro-ferroptotic role of copper. Copper increases intracellular… </p></div>
</div>
<figcaption id="figure-caption-6" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
Figure 7.
</strong>
<div class="figure-caption-contents">Role of copper in ferroptosis. (A) Pro-ferroptotic role of copper. Copper increases intracellular ROS through Fenton-like reactions or mitochondrial damage. Subsequently, increased ROS lead to lipid peroxidation of the plasma membrane or membrane structures. Furthermore, copper directly binds to GPX4 and induces GPX4 oligomerization, ultimately promoting the autophagic degradation of GPX4 mediated by the autophagy receptor TAXIBP1. (B) Anti-ferroptotic role of copper. COMMD10 is a key copper metabolism protein that reduces intracellular copper levels. Copper promotes HIF1A stabilization, thereby increasing transcription of HIF1A target genes, including FABP3, FABP7, CP, and SLC7A11. Copper-mediated upregulation of these HIF1A target genes suppresses lipid peroxidation and ferroptosis.</div>
</figcaption>
</figure>
<figure class="figure-item tail"
itemscope itemtype="http://schema.org/ImageObject"
itemprop="associatedMedia"
data-slide-index="7"
data-label-slug="figure-8">
<a class="figure-link"
href="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/60809129ebe4/KAUP_A_2200554_F0008_OC.jpg"
itemprop="contentUrl"
aria-describedby="figure-caption-7"
role="button"
data-image-width="800"
data-image-height="468"
data-image-alt="Figure 8."
data-pmc-id="PMC10351475"
data-figure-id="f0008">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-7"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/a1fe6d9e0e43/KAUP_A_2200554_F0008_OC.gif"
alt="Figure 8." />
</a>
<meta itemprop="width" itemtype="http://schema.org/ImageObject" content="800">
<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="468">
<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
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<strong class="figure-label">
<p> Figure 8. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in cuproptosis.… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 8. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in cuproptosis. Cuproptosis is induced by enrichment of copper through… </p></div>
</div>
<figcaption id="figure-caption-7" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
Figure 8.
</strong>
<div class="figure-caption-contents">Role of copper in cuproptosis. Cuproptosis is induced by enrichment of copper through SLC31A1 uptake or copper ionophores. ATP7A and ATP7B have copper efflux functions, thereby inhibting cuproptotic cell death. The cell death process is related to mitochondrial proteotoxic stress caused by lipoylation of subunites of the PDH complex, such as DLAT. FDX1 plays a key role in reducing Cu(II) to the toxic form, Cu(I), increasing DLAT protein lipidation, and promoting Fe-S cluster protein loss. Furthermore, copper-mediated damage to the mitochondrial respiratory chain causes hyperactivation of the energy sensor AMPK, which accelerates cuproptosis and the release of the pro-inflammatory mediator HMGB1.</div>
</figcaption>
</figure>
<figure class="figure-item tail"
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data-slide-index="8"
data-label-slug="figure-9">
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itemprop="contentUrl"
aria-describedby="figure-caption-8"
role="button"
data-image-width="800"
data-image-height="395"
data-image-alt="Figure 9."
data-pmc-id="PMC10351475"
data-figure-id="f0009">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-8"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/493f1c221a0c/KAUP_A_2200554_F0009_OC.gif"
alt="Figure 9." />
</a>
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<div class="figure-caption figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="caption" aria-hidden="true">
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<strong class="figure-label">
<p> Figure 9. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in autophagy.… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 9. </p>
</strong>
<div class="figure-caption-contents"><p> Role of copper in autophagy. Autophagy is a lysosome-mediated degradation process characterized by… </p></div>
</div>
<figcaption id="figure-caption-8" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
Figure 9.
</strong>
<div class="figure-caption-contents">Role of copper in autophagy. Autophagy is a lysosome-mediated degradation process characterized by the formation of multiple member structures such as phagohpores, autophagosomes, and autolysosomes. Copper can induce autophagy initiation by activating AMPK or inhibiting the MTOR kinase pathway or directly binding to ULK1 or ULK2 kinase. Copper-mediated increase in MAP1LC3 and activation of TFEB transcription factor contribute to the formation of autophagosomes and autolysosomes, respectively. Functionally, copper-induced autophagy can lead to a protective response and autophagic cell death, respectively, depending on the strength of the stimulus and the type of substrate being degraded.</div>
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data-slide-index="9"
data-label-slug="figure-10">
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itemprop="contentUrl"
aria-describedby="figure-caption-9"
role="button"
data-image-width="800"
data-image-height="615"
data-image-alt="Figure 10."
data-pmc-id="PMC10351475"
data-figure-id="f0010">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-9"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/20634776f5b5/KAUP_A_2200554_F0010_OC.gif"
alt="Figure 10." />
</a>
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<strong class="figure-label">
<p> Figure 10. </p>
</strong>
<div class="figure-caption-contents"><p> Copper chelators and ionophores in… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 10. </p>
</strong>
<div class="figure-caption-contents"><p> Copper chelators and ionophores in cancer therapy. Because copper supports the rapid growth… </p></div>
</div>
<figcaption id="figure-caption-9" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
Figure 10.
</strong>
<div class="figure-caption-contents">Copper chelators and ionophores in cancer therapy. Because copper supports the rapid growth of cancer cells, copper chelators can inhibit the functions of copper and induce apoptosis or necrosis of cancer cells. In contrast, copper ionophores transport copper into cells and induce copper overload and cytotoxicity. Copper-mediated cell death, including apoptosis, paraptosis, ferroptosis, and cuproptosis, plays a context-dependent role in tumor therapy.</div>
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itemprop="associatedMedia"
data-slide-index="10"
data-label-slug="figure-11">
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itemprop="contentUrl"
aria-describedby="figure-caption-10"
role="button"
data-image-width="800"
data-image-height="1008"
data-image-alt="Figure 11."
data-pmc-id="PMC10351475"
data-figure-id="f0011">
<img class="figure-thumb" itemprop="thumbnail"
id="article-image-10"
src="https://cdn.ncbi.nlm.nih.gov/pmc/blobs/f5d2/10351475/679aa9e22557/KAUP_A_2200554_F0011_OC.gif"
alt="Figure 11." />
</a>
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<meta itemprop="height" itemtype="http://schema.org/ImageObject" content="1008">
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<strong class="figure-label">
<p> Figure 11. </p>
</strong>
<div class="figure-caption-contents"><p> Gene expression changes in cancer… </p></div>
</div>
</div>
<div class="figure-caption-medium figure-caption-text" aria-hidden="true">
<strong class="figure-label">
<p> Figure 11. </p>
</strong>
<div class="figure-caption-contents"><p> Gene expression changes in cancer patients. The gene expression of key regulators of… </p></div>
</div>
<figcaption id="figure-caption-10" class="figure-caption-full figure-caption-text" itemtype="http://schema.org/ImageObject" itemprop="description">
<strong class="figure-label">
Figure 11.
</strong>
<div class="figure-caption-contents">Gene expression changes in cancer patients. The gene expression of key regulators of copper metabolism, cell death, and autophagy pathway in patients with cancer was analyzed using the web server GEPIA (<ext-link xmlns:xlink="http://www.w3.org/1999/xlink" ext-link-type="uri" xlink:href="http://gepia.cancer-pku.cn/">http://gepia.cancer-pku.cn/</ext-link>). Log 2 (TPM+1) was used for log-scale. ACC, adrenocortical carcinoma; BLCA, bladder urothelial carcinoma; BRCA, breast invasive carcinoma; CESC, cervical squamous cell carcinoma and endocervical adenocarcinoma; CHOL, cholangiocarcinoma; COAD, colon adenocarcinoma; DLBC, lymphoid neoplasm diffuse large Bcell lymphoma; ESCA, esophageal carcinoma; GBM, glioblastoma multiforme; HNSC, head and neck squamous cell carcinoma; KICH, kidney chromophobe; KIRC, kidney renal clear cell carcinoma; KIRP, kidney renal papillary cell carcinoma; LAML, acute myeloid leukemia; LGG, brain lower grade glioma; LIHC, liver hepatocellular carcinoma; LUAD, lung adenocarcinoma; LUSC, lung squamous cell carcinoma; MESO, mesothelioma; OV, ovarian serous cystadenocarcinoma; PAAD, pancreatic adenocarcinoma; PCPG, pheochromocytoma and paraganglioma; PRAD, prostate adenocarcinoma; READ, rectum adenocarcinoma; SARC, sarcoma; SKCM, skin cutaneous melanoma; STAD, stomach adenocarcinoma; TGCT, testicular germ cell tumors; THCA, thyroid carcinoma; THYM, thymoma; UCEC, uterine corpus endometrial carcinoma; UCS, uterine carcinosarcoma; UVM, uveal melanoma.</div>
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Steffens GC, Biewald R, Buse G.. Cytochrome c oxidase is a three-copper, two-heme-A protein. Eur J Biochem. 1987;164(2):295300.
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